Prevalence, motivation, and associated factors of medicinal herbs consumption in pregnant women from Eastern Mediterranean Regional Office: a systematic review

Abstract Context Worldwide access to medication remains a major public health problem that forces pregnant women to self-medicate with several sources, such as medicinal plants. This alternative medicine is increasing in many low- and high-income countries for several reasons. Objective This a systematic literature review on the prevalence of herbal use during pregnancy from the World Health Organization (WHO) Eastern Mediterranean Regional Office. Methods Cross-sectional studies were searched from January 2011 to June 2021 on PubMed, Scopus, and Web of Science. We used the Rayyan website to identify the relevant studies by screening the abstracts and titles. These were followed by reading the full texts to identify the final studies to be included. The data were extracted, and the quality of the studies was assessed using the quality appraisal tool. Results Of the 33 studies included in this review, 19 were conducted in Iran, 5 in Saudi Arabia, 4 in Palestine, 2 in Egypt, and 1 each in Oman, Iraq, and Jordan; the prevalence of herbal medicine use among pregnant women varied from 19.2% to 90.2%. Several plants were mentioned for pain management during the pregnancy period. The findings suggest family and friends are major motivating sources for the use of herbal medicine. Conclusions The wide variety of herbal products used in this study reflects the traditions and geographic diversity of the region. Despite the importance of literature-based data about the use of herbal medicine, it is necessary to obtain knowledge, attitude, and motivation for herbal consumption among pregnant women.


Introduction
Herbal medicines include herbs, herbal materials, herbal preparations, and finished herbal products, that contain active ingredients that are parts of plants, other plant materials, or combinations of these (World Health Organization [WHO], 2019). Herbal treatment is based on the extract of the whole plant, part of the plant (i.e., leaves, roots, flowers), or a mixture of several herbal compounds. For several years, herbal remedies have been taken as a preventive measure to maintain health and to prevent, relieve, or cure diseases (Pieroni et al. 2005). Approximately 80% of the world's population uses various traditional medicines, including herbal medicines, to diagnose, prevent, and treat disease, and to improve general well-being (Eisenberg et al. 1998). This practice is due to the popular belief that herbs are natural and free of any adverse effects compared to conventional medicine (Pieroni et al. 2005). Local traditions and social pressure, for example, high costs of drugs and medical visits, as well as insufficient health coverage, could also be the reason behind this practice (Choudhry 1997). Herbal medicines are available as non-prescription medicines. Given such ease of access, most women say that they decided to use herbal medicine on their own initiative or on the advice of family and/or friends (Kennedy et al. 2016).
In Eastern Mediterranean countries, especially in the Arab world, traditional medicine has always been practised despite the advances in modern medicine. The herbalists and scientific community have become more interested in the concept of traditional Arabic herbal medicine (Azaizeh et al. 2010). For example, an exhaustive study including 63 articles in total on Ethnobotanicopharmacological studies was carried out in Morocco, from 1991 to 2015 (Fakchich and Elachouri 2021). Another example of a research study on this subject was conducted with a specific focus on pregnant women, This work was the subject of a systematic review of herbal medicine use during pregnancy in Sub-Saharan Africa (El Hajj and Holst 2020). The first trimester of pregnancy is associated with physiological changes including nausea, vomiting, constipation, and gastric problems. In the third trimester, gastroesophageal reflux and uterine contractions are more common. Pregnant women selfmedicate by using herbs or herbal remedies to relieve the sympathetic signs of pregnancy (John and Shantakumari 2015). For this reason, women have been identified as the major users of medicinal herb products. Its prevalence is up to 60% in developed countries (Hall et al. 2011). In addition, a literature search of numerous studies from the Western world reported that the prevalence of herbal medicine use in pregnancy ranged from 1 to 60%. Moreover, the prevalence rates were 58% in the UK (Holst et al. 2011), 48% in Italy (Lapi et al. 2010), 40% in Norway (Nordeng et al. 2011), 34% in Australia (Frawley et al. 2013), and 6-9% in the USA and Canada (Moussally et al. 2009;Louik et al. 2010). These different rates of prevalence depend on geographic location, ethnicity, socioeconomic status, and cultural traditions (Illamola et al. 2019). In this context, the use of herbs during pregnancy can have deleterious consequences for the mother and fetus. It poses a major challenge for healthcare because most patients are not informed about herbal uses (Bercaw et al. 2010).
The main aims of our systematic review were to retrieve primary literature reporting the prevalence of herbal medicines used in pregnancy and the postnatal period, as well as to investigate women's experiences, motivations, and risk factors associated with the use of herbal medicines during pregnancy.

Methods
The PRISMA checklist was used to guide the reporting of the systematic review. A systematic review protocol was registered by PROSPERO 2021 with ID: CRD42021264368.

Eligibility criteria
Original articles in human studies that focused on pregnant or post-natal women based on the cross-sectional survey were considered eligible to be included in this review. Studies are also included if they describe the prevalence, attitudes, or beliefs of women towards herbal medicines or provide information about the use of herbs, and herbal products and therapies during pregnancy, including the type of herbal products, conditions of use, and source of information. We excluded unpublished reports, pilot studies, conference abstracts, opinion pieces, editorials, seminal works, and systematic reviews. Studies were excluded if they focused on women's use of herbal medicines for other conditions that were not related to maternal health care. Studies that reported the combined use of herbal medicines and drugs were excluded if the data on herbal medicines could not be separated sufficiently, and we excluded animal research.

Information sources and search strategy
Two authors, Afaf Bouqoufi and Laila Lahlou, performed independent searches on PubMed, Scopus, and Web of Science for articles published from January 2011 to 2021. The search was conducted using the Boolean operators AND OR which narrowed and widened the search and used a combination of MeSH (medical subjects heading). The following search string was used: "herbal medicine" OR plants OR «traditional medicine» OR herbs OR "herbal therapy" AND pregnancy Ã with a special focus on different countries from the Eastern Mediterranean Regional Office (EMRO).

Selection process
We used Rayyan (http://rayyan.qcri.org), a free web and mobile app, that helps expedite the initial screening of abstracts and titles using a process of semi-automation. This was followed by reading the full texts to identify the eligible studies. The references in each article were hand-searched for additional eligible studies. Finally, all articles were imported into Zotero, a bibliographic management software system.

Data collection process and data items
Using eligibility criteria, we extracted data including country of studies, year of publication, participant's demographics, the prevalence of herbal medicine use, details of herbal medicines used, characteristics of users, maternal conditions treated by herbal medicines, reasons for use, and source of information.

Study risk of bias assessment
The quality of eligible studies was assessed. This process was conducted using the Joanna Briggs Institute (JBI) 2021 an international research organization based in the Faculty of Health and Medical Sciences at the University of Adelaide, South Australia. The purpose of this appraisal is to assess the methodological quality of a study and to determine the extent to which a study has addressed the possibility of bias in its design, conduct, and analysis.
The Quality assessments were conducted by two independent authors (Afaf Bouqoufi and Laila Lahlou) using a recent version of the Joanna Briggs Institute's critical appraisal tools Checklist for Analytical Cross Sectional Studies. Critical Appraisal Tools j Joanna Briggs Institute. Joanna Briggs Institute's critical appraisal tools [Internet] j Australia: JBI; [cited 2021 August 31]. Available from: https://jbi.global/critical-appraisal-tools. A third author (Youssef Khabbal) was consulted if consensus could not be reached. When information is missing from the studies, we contacted the authors via email. All observational studies were included irrespective of quality score. The articles with missing data were included as long as they presented the prevalence of plant use. The findings of the quality appraisal of eligible studies were reported in Figure 1.

Study selection
The flowchart of the studies included in this systematic review is illustrated in Figure 2. The research generated 21,120 articles, of which 429 records were duplicates and were removed: 3459 others were excluded as ineligible after reading their titles or abstracts. Full texts of the remaining 34 records were downloaded and screened or in some cases, the full texts were screened online. After screening through the eligibility criteria, three studies were considered ineligible. A total of 31 studies were found eligible after we added two items in a simple way of research. Therefore, 33 studies were included in the systematic review.

Study characteristics
This present review includes 33 papers in total, of which 19 were conducted in Iran, 5 in Saudi Arabia, 4 in Palestine, 2 in Egypt, and 1 each in Oman, Iraq, and Jordan (Table 1). The oldest studies in terms of year of publication (2011) are in Iran (Tableaee 2011) and Oman (Al-Riyami et al. 2011). The most recent one is in Palestine (Quzmar et al. 2021). All of the included studies used structured or semi-structured survey questionnaires to collect data among pregnant women on the use of herbal medicine during pregnancy, type of herbal products, condition of use, source of information, and referral source. One study from Iran (Khadivzadeh and Ghabel 2012) employed the largest sample size of 919 women, whereas the study from Oman (Al-Riyami et al. 2011) recruited only 139 participants. The prevalence of the use of herbal medicines among pregnant women in the Eastern Mediterranean Regional Office region varied from 19.2% (Soleymani and Makvandi 2018) to 90.2% (Dabirifard et al. 2017).

Risk of bias in studies
The findings of the quality appraisal of eligible studies were reported in Figure 1. The tool is used to indicate the methodological quality and appropriateness of the observational studies, including cross-sectional studies that were reviewed in this study. It consists of eight items, and we determined the score by counting the asterisks ( Ã ) that we gave to each answer to the eight items in the grids, where a high score indicates a higher quality of study and vice versa. The six of the 33 studies were evaluated by the abstract since these articles are in Persian language and we have received no response from their authors to retrieve the full text. Two reviewers completed this process, and where there were discrepancies, a team of reviewers intervened to resolve them.

Sociodemographic characteristics of HM users
There was an important association between socio-demographic and obstetric characteristics of women and herbal medicine use. Most women in the included studies were from rural areas, homemakers, and had an educational qualification below graduation (Saadia et al. 2013;Afshary et al. 2015;Hwang et al. 2016;Botyar et al. 2018;Abdollahi et al. 2018Abdollahi et al. , 2019Yazdi et al. 2019;Raoufinejad et al. 2020). Most women in the included studies were from rural areas, homemakers, and had an educational qualification below graduation. However, a study from Saudi Arabia and Iran reported that women with a high school diploma or higher (i.e., those with at least 12 years of formal education) and women who were working full-time were significantly more likely to use herbal medicines during pregnancy compared to their less educated and unemployed counterparts (Aljofan & Alkhamaiseh 2020;Raoufinejad et al. 2020). In some studies, they found a significant relationship between age and the use of herbal medicines, with subjects aged between 20 and 29 years reporting the highest use of herbal medicines (Sattari et al. 2012;Orief et al. 2014;Botyar et al. 2018;Quzmar et al. 2021). The number of pregnancies and children also had a significant relationship with herbal medicine use, as women in their first pregnancy were mostly nonusers (Sattari et al. 2012;Quzmar et al. 2021). Two studies mentioned the association between ethnicities and herbal use (Botyar et al. 2018;Yazdi et al. 2019).
Most frequently used herbal medicines: Table 2 shows that more than half of the studies listed the types of herbal medicines used by pregnant women, whereas the other half failed to indicate the kinds of HMs used by pregnant women (Table 2). Overall, 23 studies identified a total of 67 different Quality assessment and relevance to the current study score weak: 0-3, moderate: 4-5 , strong: 6-8

NR
Reasons for use and sources of information Users of herbal medicines during pregnancy had several reasons for consuming these medicines. Informants in most of the studies reported the use of herbal medicines to alleviate pregnancyassociated symptoms. The herbs were most frequently used to treat gastrointestinal disorders such as nausea, vomiting, abdominal pain, bloating, flatulence, and stomach aches, followed by cold and flu symptoms and stretch marks. Although some others reported this use for stimulation of labor, and facilitation of childbirth. Other uses were specifically to enhance neonates intelligence and promote fetal health. Finally, skin problems, sleep disorders, and weight loss are the lesser common reasons that we have noted among some users. Finally, reported traditional indications of the most frequently used herbal medicines are shown in (Table 2). The quality and source of information received on herbal medicine automatically influence the choice of treatment for maternal illnesses. Nearly half of the reviewed materials disclosed the sources from which pregnant women received information about herbal medicines. The principal sources were family and friends respectively, for the studies (TableaTableaee 2011;Hashem Dabaghian et al. 2012;Amasha and Jarrah 2012;Khadivzadeh and Ghabel 2012;Hwang et al. 2016;Al-Ghamdi et al. 2017;Abdollahi et al. 2019;Al Essa et al. 2019;Yazdi et al. 2019;Eid et al. 2020;Raoufinejad et al. 2020;Quzmar et al. 2021). Some women decided in-person to use herbal medicines in pregnancy, labor, or postpartum (Sattari et al. 2012;Al-Ghamdi et al. 2017;Al Essa et al. 2019;Eid et al. 2020;Raoufinejad et al. 2020;Alshehri and Alshehri 2021). On the other hand, some expectant women indicated health professionals such as physicians, pharmacists, and nurses as a source of herbal medicine information (Amasha and Jarrah 2012;Hashem Dabaghian et al. 2012;Orief et al. 2014;Hwang et al. 2016;Eid et al. 2020;Raoufinejad et al. 2020;Quzmar et al. 2021;Alshehri and Alshehri 2021). Other users qbtainedtheir recommendations from the bush, traditional herbalists, the internet, social media, newspapers, radio, television, and books.

The motivation for HM utilization
The time required to decide to use HM varied greatly depending on their health needs, current knowledge, and habits. According to some studies, women's personal preferences influenced their choices and decisions. A study from Iran (Abdollahi et al. 2018) reported women's perception of the applied herb's efficacy, and 41.2% of users were fully satisfied. Women who used HM before and during gestation seemed more probable to use it throughout labor and after delivery as for example, in a study from Saudi Arabia (Afshary et al. 2015). The primary motivations to utilize herbal medicines or herbal remedies during pregnancy are that they had been taken before the pregnancy and to save money on healthcare costs. Others believe they are safe and not dangerous herbs for pregnant women and embryos (Amasha and Jarrah 2012;Khadivzadeh and Ghabel 2012;Sattari et al. 2012). Moreover, some women made decisions based on their health conditions, and according to their experiences. In Palestine, 21.0% of the participants reported that they used HM because medical therapies failed to succeed. Nearly 58% used HM because it was more accessible, compared to medical therapy. Other participants used CAM because of its common use and recommendation in their culture (Quzmar et al. 2021).

Discussion
To our knowledge, our work represents the first systematic review to identify the prevalence, motivation, and factors associated with herbal use among pregnant women in EMRO countries. This current review included 23 cross-sectional studies that included data on 13,021 women involved in the respective studies.
The findings suggest that the prevalence of herbal medicine use among pregnant women from the EMRO countries varied from 19.2% to 90.2%. This finding broadly supports the work of other studies in this area, such as a recently published systematic review by Ahmed et al. (2018) of 50 studies, including a total of 22404 African pregnant or lactating women, showing that the average prevalence of herbal medicine use during pregnancy among the different African regions was between 32% (in Central Africa) and 45% (in East Africa) (Ahmed et al. 2018). Additionally, current studies have highlighted the difference in the prevalence of herbal medicine among pregnant women, 59.3% in Yamen , 51.2%-65.6% in Ethiopia (Belayneh et al. 2022;Wake and Fitie 2022), 71.80% in Bangladesh (Jahan et al. 2022), and 67.45% in Morocco (Kamel et al. 2022). To date, many studies have investigated the impact of herbal medicine on pregnant women in another geographic area, a systematic review of Asian countries reported that, in total, 1283 out of 2729 (47.01%) women used at least one herbal medicine during their pregnancy (Ahmed et al. 2017). In Europe, North, and South America systematic review reported that, in total, 29.3% of the women (n ¼ 2673) used herbal medicines during pregnancy (Kennedy et al. 2016). Based on the survey of the literature related to our topic, some research focuses on the prevalence of herbal medicine, such as a preliminary study of pregnant women, which reported a prevalence of 57.3% (Barnes et al. 2022), a further study found that the prevalence total was 65.71% of women that used Chinese herbal medicine formulas, including 26.13% during pregnancy and 55.63% after delivery (Xiong et al. 2023).
These findings suggest that herbal medicine use during pregnancy is not only common in EMRO's countries as an entrenched part of the culture but is also common elsewhere in developed societies where traditions do not directly impact this use. Regarding the use of herbal medicine in pregnancy, most women in the studies were from rural areas, homemakers, and had an educational qualification below graduation. We found that there was a strong interplay of sociodemographic between the obstetric characteristics of women and herbal medicine use. This was in accordance with studies outside of EMRO countries that reported higher usage of herbs among women from rural areas that were less educated, these findings have been documented in previous studies in several countries around the world such as Kenya (Mothupi 2014), Bangladesh (Jahan et al. 2022), Uganda (Kaadaaga et al. 2014), and Ethiopia (Belayneh et al. 2022). In addition, it was observed that some of those women perceived that they had better knowledge about herbal medicine than the physicians/nurses and would persist in using it against medical advice. In contrast, a study in Norway and the United States shows a difference in the characteristics of herbal medicine users, the differences can be explained by the socioeconomic levels of families. The rich consult with their doctor before use or otherwise ensure adequate information about the benefits and side-effects of the herbal product (Nordeng and Havnen 2004;Bercaw et al. 2010).
The data of our systematic review contradict the widely-held hypothesis that uneducated housewives living in rural regions are the most probable users of high-risk, untested products, such as herbal or plant-based products. However, in addition to the current results, a previous study examining the prevalence of use and costs of herbal medicines in northern Scotland demonstrated that educated women were more likely to use this medicine (Pallivalapila et al. 2015). Similar findings are also reported in these studies (Mothupi 2014;Hwang et al. 2016). Based on WHO findings, twothirds of women in low-middle-income countries (LMICs) use herbal medicines as their primary source of health care (Crockett et al. 2020). Some research studies (Botyar et al. 2018;Yazdi et al. 2019) reported the relationship between ethnicities and the use of herbal medicines, these studies indicated that the Arab population used traditional medicine more than the Fars population during pregnancy. However, there is a lack of data on the use of herbal medicines among different ethnic populations worldwide (Graham et al. 2005;Rashrash et al. 2017).
The current survey showed that pregnant women from EMRO's region use a wide diversity of herbal medicine, and a total of 65 different medicinal plant species used in the traditional treatment of gestational health are reported. Generally, the African continent is known for its rich biodiversity. This species richness was reflected in the systematic review by Ahmed et al. (2018) in which the number of cited plant species varied from study to study, and 274 medicinal plants were reported to be used by African pregnant women. The following herbs were the most commonly used: (Zingiber officinale), (Thymus vulgaris), (Mentha Â piperita), (Salvia officinalis), (Matricaria chamomilla), (Trigonella foenum-graecum), (Nigella sativa), honey, (Cinnamomum verum), (Citrus Â aurantium), (Camellia sinensis), (Pimpinella anisum), (Allium sativum) and (Cuminum cyminum). The frequently used herbs in most studies were similar to other studies from the EMRO. In sub-Saharan Africa, the top herbal medicines cited in the studies were Zingiber officinale, Allium sativum, Cucurbita pepo (Cucurbitaceae), Ricinus communis (Euphorbiaceae), Vernonia amygdalina Debile (Asteraceae) and Garcinia kola Heckel (Clusiaceae). Zingiber officinale was the most common species for the treatment of pregnancy-induced nausea and vomiting and was reported in 15 studies . In contrast, due to differences in culture, traditions, and climate, it is expected that herbal medicines used during pregnancy vary across countries and regions. The herbs most commonly used in Australia (Barnes et al. 2022), Norway (Nordeng and Havnen 2004), and Tuscany were Rubus idaeus L. (Rosaceae), Foeniculum vulgare, and Hypericum perforatum L. (Hypericaceae). A good variety of reasons were proffered for using HM. The most common reason was to alleviate pregnancy-associated symptoms. The herbs were most frequently used to treat gastrointestinal disorders such as nausea, vomiting, abdominal pain, bloating, flatulence, and stomach aches, followed by cold and flu symptoms. Others reported this use for stimulation of labor or facilitation of labor and delivery. Other uses were specifically to enhance neonates' intelligence and promote fetal health. Finally, skin problems, sleep disorders, and weight loss are a few reasons that we have noted among some users. The quality and source of information obtained on herbal medicine immediately impact the choice of therapy for maternal disorders.
Family and friends were the common referral/information sources in the studies ( Tablea  . Some women decide to use herbal medicines in-person during pregnancy, labor, or postpartum. Some pregnant women, on the other hand, mentioned health professionals such as physicians, pharmacists, and nurses as source of information on herbal medicines. To provide optimal care and counseling for patients who use herbal drugs, pharmacists need to be well-informed about the use and safety of herbs and should update their knowledge. This can be achieved by providing education and training to practicing pharmacists by organizing continuing medical education programs focused on the efficacy, potential risks, possible herb-drug interactions and consequences, and the key principles applied to the administration of herbs during pregnancy. We would also advise that physicians specifically ask about herb usage and document it in the patient record. Pregnant mothers should be informed of the potential risks posed by herbs during pregnancy and advised to avoid their use. Other users obtained their recommendations from the bush, or traditional herbalists, the internet, social media, newspapers, radio, television, and books. In these cases, it is necessary to exploit this point to carry out awareness and create preventive programs, including a media campaign that uses digital conversational advertisements broadcast on sites consulted by pregnant women or those planning to become pregnant, as well as banners and videos. The multiplicity of the points of contact will ensure the visibility of this type of message to the target audience, e.g., building on the community approach with pair training that will facilitate the dissemination of the message in the community. The time taken to decide to use HM varied considerably depending on women's health needs, available information, and preferences. Some studies discovered that women's personal preferences motivated the choices and decisions they made. For most users, HM was the ideal medicine for solving pregnancy problems, inducing labor, and treating postpartum complications (Bercaw et al. 2010). Women who used HM during pregnancy and pre/pregnancy were more likely to use it during labor and after delivery. The most common reasons for using herbal medicines or herbal remedies during pregnancy are that they were using them before pregnancy, they had costly medical expenses, they are safe and harmless herbs for the mother and fetus, and they used HM because it was more accessible, compared to medical therapy. These findings were reported in other locations Sumankuuro et al. 2017;Ahmed et al. 2022;Elba et al. 2022). Moreover, some women made decisions based on their health conditions, and their experiences. The participants used herbal medicine because of its common use and recommendation in their culture. These findings were reported in other studies (Tripathi et al. 2013).

Limitations of the studies
This review contains some limitations, such as the fact that the prevalence identified may not represent the true prevalence due to the variations in the studies. Also, we have found that the majority of the published literature is predominantly from one country.

Conclusions
Overall, our systematic review is one of the first reports to shed light on the prevalence, use pattern, and perceptions of herbal medicine use among pregnant women in the EMRO's region. A low-disclosure study of herbal medicine use among pregnant women in Morocco has also been shown in the present review.
Despite the importance of literature data about the use of herbal remedies, it is necessary to obtain good knowledge, attitude, and motivation for herbal consumption among women. Healthcare professionals and researchers can disseminate the results of this study to choose the best ways to hide the message in the context of prevention. Herbal medicines may be natural, but they do contain pharmacologically active ingredients. Due to the limited number of studies, it is recommended that future studies focus on safety and the effects of herbal medicines on pregnancy outcomes.